Limited Introgression between Rock-Wallabies with Extensive Chromosomal Rearrangements

Abstract

Chromosome rearrangements can result in the rapid evolution of hybrid incompatibilities. Robertsonian fusions, particularly those with monobrachial homology, can drive reproductive isolation amongst recently diverged taxa. The recent radiation of rock-wallabies (genus Petrogale) is an important model to explore the role of Robertsonian fusions in speciation. Here we pursue that goal using an extensive sampling of populations and genomes of Petrogale from north-eastern Australia. In contrast to previous assessments using mitochondrial DNA or nuclear microsatellite loci, genomic data are able to separate the most closely related species and to resolve their divergence histories. Both phylogenetic and population genetic analyses indicate introgression between two species that differ by a single Robertsonian fusion. Based on the available data, there is also evidence for introgression between two species which share complex chromosomal rearrangements. However, the remaining results show no consistent signature of introgression amongst species pairs and where evident, indicate generally low introgression overall. X-linked loci have elevated divergence compared to autosomal loci indicating a potential role for genic evolution to produce reproductive isolation in concert with chromosome change. Our results highlight the value of genome scale data in evaluating the role of Robertsonian fusions and structural variation in divergence, speciation and patterns of molecular evolution.

Sequence Capture From Historical Museum Specimens: Maximizing Value for Population and Phylogenomic Studies

“…Dualindexed samples were barcoded with a combination of one of 96 unique p5 index sequences, and one of 24 unique p7 index sequences. For rock-wallaby samples, we used a Petrogale-specific custom exon capture approach (SeqCap EZ Developer Library; Roche NimbleGen), which targets 1.83 Mb of genomic DNA (3960 exons), designed using transcriptome data from a yellowfooted rock-wallaby (Petrogale xanthopus) (see Bragg et al, 2016;Potter et al, 2017Potter et al, , 2022. Rock-wallaby samples were indexed with a single unique barcode, and all 56 samples were pooled at equimolar ratios (1.2 µg total).…”

“…The inclusion of historical museum specimens in population genomics provides the opportunity to sample extirpated populations, potentially contributing to the delimitation of species boundaries and conservation units, assessment of extinction risk and studies of population decline (e.g., Mondol et al, 2013;Nakahama and Isagi, 2018;Nakahama, 2021). Optimizing sequence quality from historical specimens is crucial in empirical systems like Petrogale, where complex patterns of mito-nuclear discordance (Potter et al, 2012(Potter et al, , 2014, introgression (Potter et al, 2015(Potter et al, , 2017(Potter et al, , 2022, and incomplete lineage sorting across the landscape can only be resolved with comprehensive geographic sampling. In addition, data quality and completeness are especially important in studies using targeted exon capture approaches for population genomics (e.g., Bi et al, 2012;Belkadi et al, 2016;Potter et al, 2016), where there are often limited segregating sites within exonic loci.…”

A macroevolutionary role for chromosomal fusion and fission inErebiabutterflies

“…While there are some examples of studies focusing on the macroevolutionary impact of chromosomal fusions and fissions, as well as other rearrangements [ 48,49,50 ], understanding patterns of chromosome-associated speciation may require additional analysis at a finer taxonomic scale [ 40 ]. Here, we assessed the relative contributions of chromosomal fusion and fission between clades of differing ages and karyotype diversity, in order to assess the impact of these rearrangements on speciation.…”

“…Similar inferences of the impacts of chromosomal rearrangements are often carried out at higher taxonomic levels or across vast evolutionary timescales [ e.g . 61,62 ; but see 48 ], potentially masking more fine-scaled patterns in younger clades. Our study bridges between these former investigations and microevolutionary studies that focus on one species or compare sibling species [ e.g .…”

The Genetic Differentiation of Pyrrhulina (Teleostei, Characiformes) Species is Likely Influenced by Both Geographical Distribution and Chromosomal Rearrangements

“…Among animals, most cases of post-zygotic isolation are caused by genetic incompatibilities, among which chromosomal rearrangements including specific sex chromosome-systems are of fundamental importance ( Bateson, 1909 ; Dobzhansky, 1933 ; Muller, 1942 ; Coyne and Orr, 2004 ). Such chromosomal rearrangements can prevent introgression and reduce gene flow by suppressing recombination ( Machado et al, 2007 ; Yannic et al, 2009 ; McGaugh and Noor, 2012 ; Ostberg, et al, 2013 ; Presgraves, 2018 ; Potter, et al, 2021 ). However, the contribution of these processes for biodiversity in Neotropical fish species is still poorly understood.…”